A loan-out to co-star with John Wayne in the title roles of the now-classic western The Searchers (1956), began the first of three pictures he made with director John Ford; the other two being The Last Hurrah (1958) starring Spencer Tracy and as lawyer Tom Cantrell in Sergeant Rutledge (1960). The same year as The Searchers, Hunter also co-starred with top-billed Fess Parker in Walt Disney's The Great Locomotive Chase, based on an actual 1862 historical event during the American Civil War. Ironically, according to Parker's Archive of American Television interview, Ford had originally wanted to cast Parker in Hunter's role in The Searchers but Disney refused to loan him out, something Parker didn't hear about until years later; Parker referred to his loss of that part to Jeffrey Hunter as his single biggest career setback.[2]

Ford also recommended Hunter to director Nicholas Ray for the role of Jesus Christ in King of Kings (1961), a difficult part met by critical reaction that ranged from praise to ridicule. (Hunter's youthful matinee-idol looks resulted in the film's being derided as I Was a Teenage Jesus though he was thirty-four when cast in the part.)[3] Joining an all-star cast in the World War II battle epic The Longest Day, Hunter provided a climactic heroic moment playing a sergeant who is killed while leading a successful attempt to breach the defense wall atop Omaha Beach in Normandy.

Hunter described the Temple Houston that he sought to emulate as having "many sides to his character. He was a flamboyant orator; he was a bit of a dandy; he was tough; he was gentle; he was an excellent marksman," all features which gave the series greater latitude with a western format. Houston was also described as follows: He would ride, shoot, fight, drink, and love with the best of them and maybe better than most. The modesty that he displays in day-to-day life would disappear as soon as he enters a courtroom, becoming the flamboyant attorney famous throughout the American Southwest."[4]

Temple Houston proved illusory for his long-term career prospects. Hunter thought that the series had found its voice beginning with the twelfth episode, "Enough Rope", by having adopted the light-hearted approach of ABC's former Maverick western series, with James Garner.[5] As Hunter explained the change in format, the series was "conceived in humor and delivered in dead seriousness. Then, about halfway through the season, NBC decided to return to the tongue-in-cheek approach. By that time it was too late. The big joke around town was that the series was about a synagogue in Texas."[4]

Ruta Lee, who guest starred as Lucy Tolliver in "Enough Rope", said of Hunter: "He was one of the prettiest people that ever was put on the screen. God, he was gorgeous."[4] Another Hunter friend, actor Van Williams, a native of Fort Worth, who also guest starred in the series, said: "Things didn't go right for him, and they should have, because if anybody deserved to be a big star, it was Jeffrey Hunter."[4]

In taking the Temple Houston role, Hunter was compelled by a scheduling conflict to bow out of John Ford's final western film, Cheyenne Autumn.[4]

With the demise of the studio contract system in the early 1960s and the outsourcing of much feature production, Hunter, like many other leading men of the 1950s, found work in B movies produced in Italy, Hong Kong, and Mexico, with the occasional television guest part in Hollywood.[10]

Hunter's first marriage from 1950 to 1955 to actress Barbara Rush produced a son, Christopher (born 1952). From 1957 to 1967, Hunter was married to model Dusty Bartlett. He adopted her son, Steele, and the couple had two other children, Todd and Scott. In February 1969, he married actress Emily McLaughlin to whom he remained married until his death some three months later.[12]

While in Spain in 1969 to film ¡Viva América!, a story of the Chicago Mafia, Hunter was injured in an on-set explosion when a car window near him which had been rigged to explode outward instead accidentally exploded inward.[10] Hunter sustained a serious concussion. According to Hunter's third wife Emily McLaughlin, he "...went into shock" on the plane ride back to the United States after filming and "..couldn't speak. He could hardly move." After landing, Hunter was taken to Good Samaritan Hospital in Los Angeles but doctors could not find any serious injuries save for a displaced vertebra and a concussion.[13]

On the night of May 26, 1969, Hunter suffered an intracranial hemorrhage while on a three-stair set of steps at his home in Van Nuys, California.[10][13] He fell, knocked over a planter, and struck his head on a banister, fracturing his skull.[14] He was found unconscious by his wife and taken to Valley Presbyterian Hospital where he underwent brain surgery to repair his injuries, but died at about 9:30 a.m. the following morning at the age of 42.[15]

Hunter's funeral was held at St Mark's Episcopal Church in Van Nuys on May 31 after which he was interred at Glen Haven Memorial Park, in Sylmar, California.[14][16]

I am told you have decided not to go ahead with Star Trek. This has to be your own decision, of course, and I must respect it. You may be certain I hold no grudge or ill feelings and expect to continue to reflect publicly and privately the high regard I learned for you during the production of our pilot.